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J. Biol. Chem., Vol. 279, Issue 5, 3543-3552, January 30, 2004
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Epidermal Growth Factor Receptor Activation Differentially Regulates Claudin Expression and Enhances Transepithelial Resistance in Madin-Darby Canine Kidney Cells*
From the Department of Medicine, Vanderbilt University, Nashville, Tennessee 37232-4794
Tight junctions (TJs) are the most apical cell-cell junctions, and claudins, the recently identified TJ proteins, are critical for maintaining cell-cell adhesion in epithelial cell sheets. Based on their in vivo distribution and the results of overexpression studies, certain claudins, including claudin-1 and -4, are postulated to increase, whereas other claudins, especially claudin-2, are postulated to decrease the overall transcellular resistance. The overall ratio among claudins expressed in a cell/tissue has been hypothesized to define the complexity of TJs. Disruption of the TJs contributes to various human diseases, and a correlation between reduction of TJ function and tumor dedifferentiation has been postulated. The epidermal growth factor (EGF) receptor (EGFR) is overexpressed in a wide spectrum of epithelial cancers, and its expression correlates with a more metastatic cancer phenotype. However, normal functioning of EGFR is essential for normal epithelial cell proliferation and differentiation. The role of EGFR-dependent signaling in the development and maintenance of epithelial TJ integrity has not been studied in detail. This study demonstrates that, in polarized Madin-Darby canine kidney II cells, EGF-induced EGFR activation significantly inhibited claudin-2 expression while simultaneously inducing cellular redistribution and increased expression of claudin-1, -3, and -4. Accompanying these EGF-induced changes in claudin expression was a 3-fold increase in transepithelial resistance, a functional measure of TJs. In contrast, there were no alterations in protein expression and/or intracellular localization of other TJ-related proteins (ZO-1 and occludin) or adherens junction-associated proteins (E-cadherin and 
-catenin), suggesting that EGF regulates TJ function through selective and differential regulation of claudins.
Received for publication, August 6, 2003 , and in revised form, October 23, 2003.
* This work was supported by National Institutes of Health Grant DK51265 and the Department of Veterans Affairs (to R. C. H.) and by American Heart Association Southeast Affiliate Grant 4043756112-2003 (to A. B. S.). Work performed at the Vanderbilt University Medical Center Cell Imaging Core Resource was supported by National Institutes of Health Grants CA68485 and DK20593. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
To whom correspondence should be addressed: Dept. of Medicine, Vanderbilt University, C-3121 Medical Center North, Nashville, TN 37232-4794. Tel.: 615-343-0030; Fax: 615-343-7156; E-mail: ray.harris{at}vanderbilt.edu.
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